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Nephrol Dial Transplant (2007) 22: 1703–1708 doi:10.1093/ndt/gfl848 Advance Access publication 3 April 2007

Original Article

Use of pure bicarbonate-buffered peritoneal dialysis fluid reduces the incidence of CAPD peritonitis Jesu´s Montenegro, Ramo´n Saracho, Isabel Gallardo, Isabel Martı´ nez, Rosa Mun˜oz and Nuria Quintanilla Service of Nephrology, Hospital de Galdakao, Galda´cano, Vizcaya, Spain

Correspondence and offprint requests to: Jesu´s Montenegro Service of Nephrology, Hospital de Galdakao, Barrio de Labeaga s/n, E-48960 Galda´cano, Vizcaya, Spain. Email: [email protected]

Keywords: bicarbonate solution; biocompatibility of peritoneal solutions; peritoneal dialysis; peritonitis

Introduction Patients treated with peritoneal dialysis are exposed to a possible infection of the peritoneal cavity due to the presence of at least two important physioanatomical alterations associated with the dialytic technique: the non-natural communication of the peritoneal cavity with the exterior of the body through the dialysis catheter, and the repeated introduction of the dialysis fluid into the peritoneal cavity. The dialysis procedure itself is therefore a risk for peritoneal infection and even in case of skilful patients it is hard not to make any mistake during bag exchange, so that the exchange is a risk factor for dialysis peritonitis. However, access of microorganisms to the peritoneal cavity does not always cause clinical peritonitis, and it is probable that development of peritoneal infection depends on the magnitude and virulence of the bacterial inoculum and the status of peritoneal defence. Despite several modifications of the continuous ambulatory peritoneal dialysis (CAPD) technique over the last decades, including advances in bag connection technology [1,2], peritonitis remains a major source of morbidity and is the leading cause of dropout for patients maintained on CAPD therapy [3]. The peritoneal immune system plays a central role in the prevention and clearance of peritonitis in peritoneal dialysis. It has been recognized that long-term peritoneal dialysis is associated with the development of functional and structural alterations of the peritoneal membrane [4,5]. The prevalence of these alterations increases with time on peritoneal dialysis, suggesting that chronic exposure of the peritoneum to unphysiological peritoneal dialysis fluids is an important cause of functional impairment of peritoneal host defence mechanisms [6–8]. Conventional peritoneal dialysis fluids are unphysiological because of their hypertonicity, high glucose and lactate concentrations,

ß The Author [2007]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: [email protected]

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Abstract Background. Advances in bag connection technology have reduced the incidence of peritonitis in CAPD patients but there is little information on the effect of the new peritoneal dialysis fluids. Methods. We studied the incidence of CAPD peritonitis for about 3 years in 100 incident patients—50 patients dialysed with lactate-buffered solution, pH 5.5 and containing glucose degradation products (GDP) (lactate group) and 50 patients with pure bicarbonatebuffered solution, pH 7.4 and low GDP (bicarbonate group). Patients in both groups were similar in age, sex, length of time on CAPD, connection technology and handling of dialysis. Results. In the lactate group, 74 episodes of peritonitis were recorded compared with 43 in the bicarbonate group, i.e. one episode per 21 patient-months with the lactate dialysis fluid and one episode per 36 patient-months with the bicarbonate dialysis fluid (OR 0.58, 95% CI 0.37–0.91, P ¼ 0.017). A total of 3369 exchanges per episode of peritonitis were recorded for bicarbonate compared with 2004 exchanges per episode of peritonitis in the lactate group. The majority of organisms isolated in both groups were Gram-positive bacteria, with a predominance of the oropharyngeal and cutaneous endogenous flora. Three episodes of fungal peritonitis occurred in the lactate group and none in the bicarbonate group. Conclusions. Our results suggest that the pure bicarbonate-buffered peritoneal dialysis fluid appears to reduce the frequency of peritonitis in CAPD patients possibly in relation to greater biocompatibility and maintenance of peritoneal membrane structural integrity. Similar results can probably relate to all low-GDP solutions.

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Materials and methods An open, non-randomized, prospective, observational study was designed to compare the incidence of peritonitis in patients starting CAPD according to the type of dialysate fluid used from the start of peritoneal dialysis (lactatebuffered vs bicarbonate-buffered). The study was performed in a dialysis unit of an acute-care teaching hospital in Spain. The study was conducted in accordance with Good Clinical Practice standards, and prior to study initiation, the Ethics Committee of the hospital was notified of the study protocol. Written informed consent was obtained from all participants. Patients were divided into the group of conventional lactate-buffered solution (lactate group), in which CAPD was performed with a double-bag system and a peritoneal dialysis fluid with 35 mM lactate, pH 5.5 and containing GDP (StaySafeÕ , Fresenius Medical Care, Bad Homburg, Germany) and the group of pure bicarbonate-buffered solution (bicarbonate group), in which CAPD was performed with a double-chamber bag and a peritoneal dialysis fluid with 34 mM bicarbonate, pH 7.4 and low GDP (BicaVeraÕ , Fresenius Medical Care). The same Stay-Safe peritoneal dialysis system (Fresenius Medical Care) using Biofine as well as PIN (automatic inline-closing procedure minimizing the risk of contamination during bag disconnection) and DISC technology was used in both study groups. The lack of availability at any moment during the study period of the new bicarbonate-buffered dialysate fluid prevented the study from being designed as a randomized trial. A convenient sample of 50 incident patients in each group with duration of follow-up of at least 1 year was selected. The selection of patients for the study began on 1 January 1999, when the new bicarbonate-buffered dialysate fluid became available at our centre. Availability of the bicarbonate-buffered dialysate

fluid was intermittent at the commencement of the study, with full availability thereafter. When sufficient bags of bicarbonate-buffered dialysate fluid were available, the patient was dialysed with bicarbonate-buffered solution; when bags of bicarbonate-buffered dialysate fluid were not available, the patient was dialysed with standard lactatebuffered solution. On 30 June 2004, a total of 50 patients had been dialysed with lactate-buffered solution and had completed at least 1 year on dialysis treatment. Since that date, all patients were dialysed with bicarbonate-buffered solution up to January 2005, when the number of 50 patients assigned to the bicarbonate group was reached. In none of the patients was the initial dialysis solution changed to the other. The selection process ended in January 2005 and the observation period in January 2006. All patients were trained by the same nursing team, and after training and periodically, different parameters related to skills, discipline and ability in handling of the procedure, especially exchanges, were assessed using a 3-point ordinal scale from 1 ¼ bad, 2 ¼ regular and 3 ¼ good. The protocol of peritoneal catheter insertion was the same for all patients, including antibiotic prophylaxis, implantating physician and fast flow swan neck curled peritoneal dialysis catheter (Fast FlowÕ , Fresenius Medical Care). Nasal carriers of Staphylococcus aureus were treated with intranasal mupirocin. Routine exit-site care consisted of daily washing with antibacterial soap and thorough drying using a hair dryer. In case of suspicion of exit-site infection or in the presence of risk factors for exit-site infection, ciprofloxacin otological solution (a single-dose vial of 0.5 ml ciprofloxacin, 1 mg) was applied daily around the insertion site [16]. Peritonitis was defined as appearance of abdominal symptoms, cloudy effluent with 100/ml white cells with 50% of these polymorphonuclear cells, and positive and negative growth after seeding uncentrifuged (10 ml) and centrifuged (sediment of 50 ml centrifuged and resuspended in 20 ml of distilled water) dialysate into aerobe/anaerobe haemoculture bottles [17]. Patients with peritonitis were admitted to the hospital for in-patient care. The initial empirical antibiotic regimen for the treatment of peritonitis consisted of intraperitoneal vancomycin and ceftazidime, and the antibiotic regimen was then adjusted according to the culture and sensitivity results when available. Response was assessed by the disappearance of symptoms and signs of peritonitis and the clearing of peritoneal effluent. Other data recorded during the study period in addition to the episodes of CAPD peritonitis included the Charlson Comorbidity Index at the beginning of CAPD, residual renal function (RRF), blood cell count, biochemical profile, C-reactive protein, protein catabolism, renal urea and creatinine clearances, Kt/V urea, number of exchanges, number of hypertonic bags, reasons for CAPD cessation and all circumstances related to the patient of the procedure prior to the appearance of peritonitis considered risk factors for peritoneal infection, such as forgotten use of disposable surgical mask, connector portions touching anything, bag rupture, gastrointestinal status (constipation, diarrhoea), etc.

Statistical analysis Peritonitis rate was estimated as the patient-months number, the patient-years number and the patient-exchanges number

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acidic pH and presence of glucose degradation products (GDP) [9]. The recognition that dialysate bioincompatibility has adverse effects on peritoneal structure and function has given impetus to the development of new peritoneal dialysis fluids. New peritoneal dialysate fluids have been developed with pH-adjustment to physiological values, use of bicarbonate as buffer system and markedly reduced GPD levels through the use of double-chamber bags [10,11]. The new dialysate fluids may exert less suppressive effects on peritoneal leucocyte function. Various in vitro studies have shown that conventional peritoneal dialysis fluids compromise the function of leucocytes, peritoneal mesothelial cells and phagocytic cells [12–14]. The available data indicate that exposure of the peritoneal environment to more compatible peritoneal dialysis solutions is associated with improvements of peritoneal cell function, alterations in markers of membrane integrity and reduced local inflammation [15]. The objective of this study was to determine the incidence of peritonitis in CAPD patients using a purely bicarbonate-based, neutral-pH peritoneal dialysis fluid in comparison with a conventional lactate-buffered acidic fluid.

J. Montenegro et al.

Potentially favourable effects of pure bicarbonate dialysis fluid on CAPD peritonitis

per episode. Differences in the incidence of CAPD peritonitis between the study groups were assessed using a negative binomial regression model. Peritonitis rate has been shown to have a Poisson distribution in peritoneal dialysis patients. In the univariate analysis, the chi-square (2) test or the Fisher’s exact test were used for the comparison of categorical variables. Continuous variables were compared by the Student’s t-test. A P-value of 0.05 or less was considered statistically significant. Confidence intervals were calculated for 95%. Results are expressed as mean (SD) unless otherwise stated. The SAS system software package (SAS Institute Inc., Cary, NC) version 8.2 for Windows was used for the analysis of data.

Results

Table 1. Demographic data of recruited patients Data

Age, years, mean (SD) Male/female ratio Duration of dialysis, days, mean (SD) Primary renal disease Glomerulonephritis Diabetes mellitus Interstitial nephritis Nephroangiosclerosis/ Ischaemic nephropathy Others

Lactate (n ¼ 50)

Bicarbonate (n ¼ 50)

60.1 (14.6) 35/15 907 (438)

61.1 (15.3) 34/16 917 (387)

11 5 20 9

18 11 5 12

5

4

two in the lactate group and one in the bicarbonate group. Culture-negative episodes are included in the analysis. As shown in Figure 1, most episodes in both groups developed during the first year of CAPD, with more episodes of peritonitis per patient in the lactate group. The incidence of CAPD peritonitis was higher in the lactate group than in the bicarbonate group (0.60 vs 0.34 episodes per patient-years, or one episode per 1.68 patient-years vs one episode per 2.92 patientyears) (Table 2). These differences were statistically significant in the initial unadjusted regression model (OR ¼ 0.58 95% CI, 0.370.91, P ¼ 0.017), that is, the risk for CAPD peritonitis was 42% lower in patients treated with the new bicarbonate-buffered dialysis fluid compared with the conventional lactate-buffered fluid. In the regression model adjusted by age, sex, CAPD

Lactate

Bicarbonate

6

5

4

3

2

1 0 0 1 Years of follow-up

2

3

4

5

6

Fig. 1. Patients in both groups (solid line), years of follow-up and episodes and date of peritonitis (filled circle).

Table 2. Incidence of CAPD peritonitis and reasons for CAPD cessation Data

Lactate (n ¼ 50)

Bicarbonate P (n ¼ 50)

Peritonitis, no. of episodes Duration of cloudy fluid, h, mean  SD Peritonitis rate, patient-years/ patient-months Peritonitis-free patients, no. Exchanges, no. Peritonitis rate per 1000 exchanges Exchanges per episode of peritonitis, no. Reasons for CAPD cessation Transplantation Haemodialysis Automated peritoneal dialysis Death Others

74a 39  12

43b 53  22

a

Two culture-negative episodes. One culture-negative episode

b

0.021 0.007

0.60/20.4 0.34/35.5

0.017

21 148 300 0.50 2004

24 144 900 0.30 3369

NS NS 0.021 0.021

18 7 4 17 2

13 6 2 7 2

NS NS NS 0.0025 NS

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One hundred patients were recruited and assigned to 50 patients in each group (the lactate group and the bicarbonate group). Table 1 shows the demographic and clinical parameters of the patients. The two groups were similar in age, sex ratio and dialysis-therapy duration. Blood cell count and protein catabolism were similar in both groups. Diabetes mellitus and glomerulonephritis were more frequent in the bicarbonatebuffered group, whereas interstitial nephritis was more common in the conventional lactate-buffered group. Regarding the ability for handling the peritoneal dialysis procedure, similar rates were obtained in both groups and the majority of patients were qualified. Twenty-nine patients in the lactate group and 28 in the bicarbonate group used hypertonic bags. The total number of bag exchanges, calculated by patient records, were slightly higher in the lactate group (n ¼ 148 300) than in the bicarbonate group (n ¼ 144 900). At the beginning of CAPD, there were 18 nasal carriers of S. aureus in the bicarbonate group and 17 in the lactate group, with recurrences in 8 and 11 patients, respectively. The number of events considered at risk for CAPD peritonitis was also similar—21 in the lactate group and 25 in the bicarbonate group. In the lactate group, 74 episodes of peritonitis were recorded compared with 43 in the bicarbonate group. There were three cases of culture-negative peritonitis,

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J. Montenegro et al.

Table 3. Organisms isolated and negative culture in patients with CAPD peritonitis Data

Lactate

Gram-positive organisms Staphylococcus epidermidis Other coagulase-negative Staphylococci Staphylococcus aureus Streptococcus spp. Enterococcus spp. Gram-negative organisms Enterobacterias spp. Aeromonas spp. Proteus spp. Klebsiella spp. Hafnia alvei Cytrobacter spp. Fungi Candida spp. No growth

ml/m 14 12 10 8 6 4 2 0

Lactate

RRF initial

RRF final

No.

Gram (%)

Total (%)

No.

Gram (%)

Total (%)

25 14 4 14 1

43 24 7 24 2

35 19 6 19 1

11 8 4 12 0

31 23 12 34 0

27 19 10 28 0

6 0 2 2 0 1

55 0 18 18 0 9

9 0 3 3 0 1

4 2 0 0 1 0

57 29 0 0 14 0

9 5 0 0 2 0

4 3

0 1

3 2

Bicarbonate

Table 4. Results of laboratory test at the initiation of CAPD and at the end of the study Data

RRF initial

RRF final

Fig. 2. Initial and final RRF of study, better preserved in BicaVera group (P ¼ 0.004).

ability-skills, nasal carrier of S. aureus, aetiology of primary renal disease and weekly Kt/V urea, the results obtained for the bicarbonate group were similar (OR ¼ 0.64, 95% CI 0.430.96, P ¼ 0.029). When results were expressed as patient-exchanges, the incidence of CAPD peritonitis was 0.50 episodes per 1000 patient-exchanges in the lactate group compared with 0.30 in the bicarbonate group. Significant differences were obtained in the unadjusted (OR ¼ 0.59, 95% CI 0.37–0.92, P ¼ 0.021) and adjusted (OR ¼ 0.65, 95% CI 0.430.98, P ¼ 0.038) negative binomial regression models. As shown in Table 3, the majority of organisms isolated in both groups were Gram-positive bacteria (80.5% lactate group and 84% bicarbonate group), with a predominance of the coagulase-negative Staphylococci. Three episodes of Candida spp. peritonitis occurred in the lactate group and none in the bicarbonate group. Differences in the mean (SD) leucocyte count of the initial peritoneal samples were not observed [2782 (883) leucocytes/mm3 in the lactate group vs 2845 (907) leucocytes/mm3 in the bicarbonate group] but duration of cloudy effluent and disappearance of peritoneal leucocytes to normal values was significantly shorter in patients dialysed with the new bicarbonate than in those with conventional lactate (48  16 vs 64  29 h, P ¼ 0.015).

0 2

Residual renal function Initial Final Prealbumin, mg/dl Initial Final n-pcr urea Initial Final Albumin, g/dl Initial Final C-reactive protein, mg/dl Initial Final

Lactate (n ¼ 50)

Bicarbonate (n ¼ 50)

7.07 (1.5) 2.29 (2.18)*

7.05 (1.8) 4.13 (3.38)

32 (4) 34 (2)

30 (3) 33 (5)

1.4 (0.3) 1.3 (0.2)

1.3 (0.3) 1.4 (0.4)*

3.9 (0.5) 3.5 (0.5)

3.6 (0.4) 3.5 (0.6)

2.68 (2.83) 4.14 (3.83)*

2.64 (2.63) 2.39 (2.35)

Data as mean (SD). *P < 0.05.

The most common reason for CAPD cessation was renal transplantation (Table 2). Five patients in the lactate group and one patient in the bicarbonate group required haemodialysis initiation because of torpid, recurrent peritonitis or fungal peritonitis. A significantly higher number of patients in the lactate group (n ¼ 17) than in the bicarbonate group (n ¼ 7) had CAPD cessation because of death, although the Charlson Comorbidity Index at the initiation of CAPD was lower in the lactate group, 20 vs 35% in group 0. At the end of CAPD, RRF was significantly lower in the lactate group (P ¼ 0.004) (Figure 2) and serum C-reactive protein concentration was significantly higher (P < 0.05). n-pcr urea improved significantly in the bicarbonate group (P < 0.05) but differences with regard to other variables were not observed (Table 4).

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ml/m 14 12 10 8 6 4 2 0

Bicarbonate

Potentially favourable effects of pure bicarbonate dialysis fluid on CAPD peritonitis

Discussion

peritoneal dialysis Moreover, the number of events considered risk factors for peritonitis was similar in both groups but even with a higher percentage in the bicarbonate group (49 vs 30%). Nasal Staphylococcus carrier status is related to the development of staphylococcal peritonitis [20]. In our study, although the number of nasal carriers of S. aureus was similar in both groups, only four patients in each group developed staphylococcal peritonitis, probably due to the meticulous exit-site care protocol of our dialysis unit [16]. On the other hand, a shorter duration of cloudy effluent in the bicarbonate group supports more preserved peritoneal defence mechanisms due to dialysate biocompatibility. In a prospective, randomized study of patients in automated peritoneal dialysis to compare the biocompatibility of either conventional solution or bicarbonate/lactate neutral fluid (PhysionealÕ , Baxter HealthCare) over 5 months, the use of a neutral solution improved biocompatibility parameters reflecting enhanced phagocytotic activity of peritoneal macrophages, reduced constitutive inflammatory stimulation (IL-6), reduced accumulation of advanced glycosylation end-products in the peritoneal cavity and better preservation of the mesothelial cell integrity [21]. The majority of organisms isolated in both groups were Gram-positive bacteria, with a predominance of coagulase-negative Staphylococci followed by Streptococcus spp. These pathogens that form part of the oropharyngeal and cutaneous flora accounted for >70% of CAPD peritonitis in both groups. This confirms the importance of the intraluminal catheter route for bacterial invasion and the development of peritonitis. Since there were no differences between the study groups in the ability for handling the procedure and risk factors for peritonitis, the lower incidence of CAPD peritonitis in the bicarbonate group also indicates the more favourable effects of dialysate biocompatibility on the natural defence mechanisms of the peritoneum. Three episodes of fungal peritonitis occurred in the lactate group and none in the bicarbonate group. Preservation of dendritic cell differentiation and function [22] under pure bicarbonate conditions may explain the absence of fungal peritonitis in the bicarbonate group. In a randomized, prospective, controlled, open-label study comparing a bicarbonate/lactate with a standard lactate-buffered peritoneal dialysis solution over a 12-month treatment period, the overall peritonitis rates with the new solution appeared to be largely unaffected by the nature of the buffer, but in patients who continued into the long-term phase of the study, there was a significant difference between the peritonitis rates in the bicarbonate/lactate and control groups (1/51 vs 1/19) [23]. In our study, although no case of CAPD peritonitis-related death was observed, a significantly higher number of patients in the lactate group than in the bicarbonate group had CAPD cessation because of death, although the Charlson Comorbidity Index at the initiation of CAPD was lower in the lactate group. New biocompatible

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The main finding of the study is a significantly lower rate of CAPD peritonitis in the group of patients dialysed with the new bicarbonate-buffered fluid compared with those dialysed with the conventional lactate-buffered dialysis fluid. This reduction in the incidence of episodes of peritonitis seems attributable to differences in the composition of the dialysate fluid, given that patients in both study groups were comparable in terms of risk factors for peritonitis. Both groups were homogeneous according to demographic characteristics and duration of dialysis. At the start of CAPD, the Charlson Comorbidity Index was lower in patients in the lactate group, which may be explained by a lower number of diabetes and a higher number of interstitial nephropathies as the primary renal disease among these patients. However, the mortality during the study was higher in the lactate group than in the bicarbonate group. It should be noted that the main limitation of the study is the fact that it is not randomized. The nutrition status was adequate in both groups, and patients dialysed with bicarbonate showed a higher protein intake according to the protein catabolism; however, marked differences in other variables either at the beginning or at the end of the study were not observed. Nutritional variables were unrelated to CAPD peritonitis except for serum albumin levels. We studied a sample of incident patients who started CAPD with some degree of RRF. It has been reported that RRF is better preserved with the use of biocompatible solutions with low GDP [18] compared with patients dialysed with an acidic dialysis fluid, lactate-buffered and GDP in which RRF vanishes more rapidly than in patients dialysed with bicarbonate-buffered fluids, as previously reported [19]. A faster decline of RRF in patients receiving the StaySafe dialysis fluid has a negative impact on bag exchanges. Main risks for CAPD peritonitis occur during bag exchange. It may be argued that exposure to a higher number of bag exchanges may account for a greater number of episodes of peritonitis. However, an odds ratio of 0.59 in favour of the bicarbonate group was obtained in the regression models when data were expressed as patient-years or patient-exchanges. Because the dialysis system was the same for all patients and the number of exchanges was not related to a higher incidence of peritonitis, it can be argued that characteristics of the dialysate fluid in the bicarbonate group should be directly associated with a reduction of the number of CAPD peritonitis in this group. Other factors that exert an effect on the incidence of CAPD peritonitis are related to the ability and skills in handling of the procedure. However, the percentages of patients rating their ability as ‘bad’, ‘regular’ or ‘good’ were similarly distributed in both study groups. Differences in the number of episodes of CAPD peritonitis were already evident at the first year on

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peritoneal dialysis fluids that appear to preserve peritoneal function may improve patient survival [24]. These results are compatible with a beneficial impact of pure bicarbonate, low-GDP peritoneal dialysis solutions on peritonitis rates. Whether this effect is a brand-specific advantage, or is attributable to all lowGDP solutions, remains to be resolved. Acknowledgement. We thank Marta Pulido, MD, for editing the manuscript and editorial assistance. Conflict of interest statement. None declared.

References

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